Helical Fungi Under Physical Constraints*

Helical filaments are represented in living organisms from the molecular to the multi-cellular scale. Described by Darwin in aerial and underground parts of plants as early as the 19th century, they still raise fundamental questions about their roles and their underlying mechanisms. We here focus on the oscillatory shapes adopted by the filaments (hyphae) of the fungus Candida albicans in different conditions of physical constraints such as z-confinement. Microfluidic channels presenting successive portions of different heights, lower and higher the hyphal diameter (2 µm), allow the observation of a reversible geometrical transition between planar wavy shapes and helices. Interestingly, 2D oscillations are created by successive shifts and deformations of the distal part of the hypha, occurring periodically after short periods of rather rectilinear growth. In both helices and wavy shapes, the cell wall is asymmetrically thicker/denser in the inner part of the curvature, suggesting a periodic re-orientation of the vesicle supply center during hyphal growth. We have also evaluated the possible advantages of these oscillatory growth modalities in the colonization of complex spaces by implementing micro-pillar arrays in microfluidic devices. The hyphae navigate through these networks of obstacles by making successive coordinated choices among the 3 possibilities offered at the corner of each individual obstacle. Strikingly, for optimized maze geometries, hyphae preferentially change their curvature at each step, drawing regular oscillations along a constant growth direction. This phenomenon of directional memory, which highlights an elementary sense of proprioception in these filamentous organisms, and the dynamic formation of curvatures through localized morphological relaxation near the apex are in line with the concept of squeelix ("squeezed helix") involving filament bending and twisting energies.